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Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators

ABSTRACT: We report that ancestral zinc-finger-domain transcriptional regulators, previously reported to control virulence/symbiosis, implement a cell cycle (S→G1) transcriptional switch. To unravel how this G1-phase transcriptional program is reinstated during a primitive cell cycle, we first defined G1-specific promoters in the model bacterium Caulobacter crescentus by comparative ChIP-Seq analysis. We then exploited one such promoter as genetic proxy, to identify two conserved developmental regulator paralogs, MucR1/2, that constitute a quadripartite and homeostatic regulatory module directing the switch from S→G1-phase transcription. Surprisingly, MucR orthologs that regulate virulence and symbiosis gene transcription in Brucella, Agrobacterium or Sinorhizobium support the G1 transcriptional switch in Caulobacter. Pan-genomic ChIP-Seq analyses in Sinorhizobium and Caulobacter show that this module targets orthologous genes. Thus, this ancestral bacterial lineage from which eukaryotic organelles descended may coordinate virulence/symbiosis with other cell cycle functions using a primordial transcription factor fold that is now primarily found in the eukaryotic domain of life.

ORGANISM(S): Caulobacter vibrioides Sinorhizobium fredii

PROVIDER: GSE52849 | GEO | 2014/05/25

SECONDARY ACCESSION(S): PRJNA230623

REPOSITORIES: GEO

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Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators

Project description:We report that ancestral zinc-finger-domain transcriptional regulators, previously reported to control virulence/symbiosis, implement a cell cycle (SM-bM-^FM-^RG1) transcriptional switch. To unravel how this G1-phase transcriptional program is reinstated during a primitive cell cycle, we first defined G1-specific promoters in the model bacterium Caulobacter crescentus by comparative ChIP-Seq analysis. We then exploited one such promoter as genetic proxy, to identify two conserved developmental regulator paralogs, MucR1/2, that constitute a quadripartite and homeostatic regulatory module directing the switch from SM-bM-^FM-^RG1-phase transcription. Surprisingly, MucR orthologs that regulate virulence and symbiosis gene transcription in Brucella, Agrobacterium or Sinorhizobium support the G1 transcriptional switch in Caulobacter. Pan-genomic ChIP-Seq analyses in Sinorhizobium and Caulobacter show that this module targets orthologous genes. Thus, this ancestral bacterial lineage from which eukaryotic organelles descended may coordinate virulence/symbiosis with other cell cycle functions using a primordial transcription factor fold that is now primarily found in the eukaryotic domain of life. Examination of 5 transcripton factor binding in two different species

2014-05-25 | E-GEOD-52849 | biostudies-arrayexpress

Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators

Project description:Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators

| PRJNA230623 | ENA

Developmental switch within the bacterial cell cycle regulator CtrA

Project description:Many bacteria acquire dissemination and virulence traits in G1-phase. CtrA, an essential and conserved cell cycle transcriptional regulator identified in the dimorphic alpha-proteobacterium Caulobacter crescentus, mysteriously switches from activating promoters in late S-phase to a different set in G1-phase. We found that a core and highly conserved determinant in the DNA-binding domain (DBD) of CtrA governs this promoter switch and that it is also required for promoter reprogramming in stationary phase in response to a (p)ppGpp alarmone signal perceived by the RNA polymerase beta subunit. A simple side chain modification in one critical residue of this DBD confers opposing developmental phenotypes and transcriptional activities. This region is also central to understanding the developmental reprogramming in the obligate intracellular Rickettsiae where replicative cells develop into dispersal cells and a naturally occurring polymorphism in the rickettsial DBD resembles a mutation that drives CtrA towards activation of the dispersal (G1-phase) program in Caulobacter.

2019-11-25 | GSE134017 | GEO

Bypass of an epigenetic S-phase transcriptional module by convergent nutrient stress signals

Project description:The signals feeding into bacterial S-phase transcription are poorly understood. Cellular cycling in the alpha-proteobacterium Caulobacter crescentus is driven by a complex circuit of at least three transcriptional modules that direct sequential promoter firing during the G1, early and late S cell cycle phases. In alpha-proteobacteria, the transcriptional regulator GcrA and the CcrM methyltransferase epigenetically activate promoters of cell division and polarity genes that fire in S-phase. By evolving Caulobacter crescentus cells to cycle and differentiate in the absence of the GcrA/CcrM module, we discovered that phosphate deprivation and (p)ppGpp alarmone stress signals converge on S-phase transcriptional activation. The cell cycle oscillations of the CtrA protein, the transcriptional regulator CtrA that implements G1 and late S-phase transcription, are essential in our evolved mutants, but not in wild-type cells, showing that the periodicity in CtrA abundance alone can sustain cellular cycling without GcrA/CcrM. While similar nutritional sensing occurs in other alpha-proteobacteria, GcrA and CcrM are not encoded in the reduced genomes of obligate intracellular relatives. We thus propose that the nutritional stress response induced during intracellular growth obviated the need for an S-phase transcriptional regulator.

2023-11-09 | GSE135899 | GEO

Polymerase occupancy (ChIP-Seq) in WT and mutants of Caulobacter crescentus NA1000

Project description:Coordination of cell cycle progression with central metabolism is fundamental to all cell types and likely underlies differentiation into dispersal cells in bacteria. How central metabolism is monitored to regulate cell cycle functions is poorly understood. A forward genetic selection for cell cycle regulators in the polarized alpha-proteobacterium Caulobacter crescentus unearthed the uncharacterized CitA citrate synthase, a TCA (tricarboxylic acid) cycle enzyme, as unprecedented checkpoint regulator of the G1→S transition. We show that loss of the CitA protein provokes a (p)ppGpp alarmone-dependent G1-phase arrest without apparent metabolic or energy insufficiency. While S-phase entry is still conferred when CitA is rendered catalytically inactive, the paralogous CitB citrate synthase has no overt role other than sustaining TCA cycle activity when CitA is absent. With eukaryotic citrate synthase paralogs known to fulfill regulatory functions, our work extends the moonlighting paradigm to citrate synthase coordinating central (TCA) metabolism with development and perhaps antibiotic tolerance in bacteria.

2020-03-19 | GSE144533 | GEO

In-phase oscillation of global regulons is orchestrated by a pole-specific organizer

Project description:Cell fate determination in the asymmetric bacterium Caulobacter crescentus (Caulobacter) is triggered by the localization of the developmental regulator SpmX to the old (stalked) cell pole during the G1-S transition. While SpmX is required to localize and activate the cell fate-determining kinase DivJ at the stalked pole in Caulobacter, it is also required for organelle (stalk) positioning in the cousin Asticaccaulis. We unearth the conserved s54-dependent transcriptional activator regulator TacA as global regulator in Caulobacter whose activation by phosphorylation is indirectly down-regulated by SpmX. Using a combination of forward genetics and cytological screening we uncover a previously uncharacterized and polarized component (SpmY) of the TacA phosphorylation control system, and we show that the SpmY function and localization is conserved. Thus, we demonstrate that SpmX organizes a site-specific, ancestral and multi-functional regulatory hub whose function includes the coordinated control of two co-oscillating global transcriptional regulators, CtrA and TacA.

2016-10-24 | GSE85186 | GEO

The Conserved Polarity Factor PodJ1 Impacts Multiple Cell Envelope-Associated Functions in Sinorhizobium meliloti

Project description:Although diminutive in size, bacteria possess highly diverse and spatially confined cellular structures. Two related alpha-proteobacteria, Sinorhizobium meliloti and Caulobacter crescentus, serve as models for investigating the genetic basis of morphologic variations. S. meliloti, a symbiont of leguminous plants, synthesizes multiple flagella and no prosthecae, whereas C. crescentus, a freshwater bacterium, has a single polar flagellum and stalk. The podJ gene, originally identified in C. crescentus for its role in polar organelle development, is split into two juxtaposed open reading frames, podJ1 and podJ2, in S. meliloti. Deletion of podJ1 interferes with flagellar motility, exopolysaccharide production, cell envelope integrity, cell division, and normal morphology, but not symbiosis. As in C. crescentus, the S. meliloti PodJ1 protein appears to act as a polarity beacon and localizes to the newer cell pole. Microarray analysis indicates that podJ1 affects the expression of at least 129 genes, the majority of which correspond to observed mutant phenotypes. The combination of phenotypic characterization, microarray analysis, and suppressor identification suggests that PodJ1 controls a core set of conserved elements, including flagellar and pili genes, the signaling proteins PleC and DivK, and the TacA transcriptional activator, while alternate downstream targets have evolved to suit the distinct lifestyles of individual species. Gene expression profiling of Sinorhizobium meliloti Rm1021 or its isogenic podJ1 deletion mutant, grown to mid exponential phase in rich medium, was performed using custom Affymetrix GeneChips.

2012-08-09 | E-GEOD-31325 | biostudies-arrayexpress

Expression analysis of Sinorhizobium meliloti 1021rpoH1 rpoH2 mutant during heat shock

Project description:Investigation of whole genome gene expression level changes in a Sinorhizobium meliloti 1021 rpoH1 rpoH2 double mutant, compared to the wild-type strain. The mutations engineered into this strain render it deficient in symbiotic nitrogen fixation. The mutants analyzed in this study are further described in Mitsui, H, T. Sato, Y. Sato, and K. Minamisawa. 2004. Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa. Mol Gen Genomics 271:416-425.

2014-11-01 | GSE62900 | GEO

Overexpression of cyaJ in Rm2011 to study effects of increased cAMP on the transcriptome of Sinorhizobium meliloti

Project description:Alpha-rhizobia are soil-dwelling alphaproteobacteria existing either in free-living states or in symbiosis with a leguminous plant host. cyaJ is a putative adenylate/guanylate cyclase transmembrane protein. Overexpression of cyaJ leads to increased > levels of cAMP. To investigate the effect of increased cAMP on the transcriptome of Sinorhizobium meliloti we performed microarray analysis of > Sinorhizobium meliloti Rm2011 carrying an empty vector pWBT or cyaJ overexpression construct pWBT-cyaJ.

2016-08-17 | E-MTAB-4932 | biostudies-arrayexpress

The small proteome of the nitrogen-fixing plant symbiont Sinorhizobium meliloti

Project description:The Alphaproteobacterium Sinorhizobium meliloti lives in soil and is capable of fixing molecular nitrogen in symbiosis with legume plants. In this work, the small proteome of S. meliloti strain 2011 was studied to uncover translation of both annotated and novel small open reading frame (sORF)-encoded proteins (SEPs).

2023-03-13 | PXD034931 | Pride

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